https://hdl.handle.net/10481/32042 2026-04-11T18:38:23Z 2026-04-11T18:38:23Z Van der Zee, Romee Gomez-Moracho, Tamara Pisa, Lisa Sagastume, Soledad García-Palencia, Pilar Maside, Xulio Bartolomé, Carolina Martín-Hernández, Raquel Higes, Mariano https://hdl.handle.net/10481/111451 2026-02-24T09:12:55Z

Virulence and polar tube protein genetic diversity of Nosema ceranae (Microsporidia) field isolates from Northern and Southern Europe in honeybees (Apis mellifera iberiensis) Van der Zee, Romee; Gomez-Moracho, Tamara; Pisa, Lisa; Sagastume, Soledad; García-Palencia, Pilar; Maside, Xulio; Bartolomé, Carolina; Martín-Hernández, Raquel; Higes, Mariano Infection of honeybees by the microsporidian Nosema ceranae is considered to be one of the factors underlying the increased colony losses and decreased honey production seen in recent years. However, these effects appear to differ in function of the climatic zone, the distinct beekeeping practices and the honeybee species employed. Here, we compared the response of Apis mellifera iberiensis worker bees to experimental infection with field isolates of N. ceranae from an Oceanic climate zone in Northern Europe (Netherlands) and from a Mediterranean region of Southern Europe (Spain). We found a notable but non-significant trend (P = 0.097) towards higher honeybee survival for bees infected with N. ceranae from the Netherlands, although no differences were found between the two isolates in terms of anatomopathological lesions in infected ventricular cells or the morphology of the mature and immature stages of the parasite. In addition, the population genetic survey of the N. ceranae PTP3 locus revealed high levels of genetic diversity within each isolate, evidence for meiotic recombination, and no signs of differentiation between the Dutch and Spanish populations. A cross-infection study is needed to further explore the differences in virulence observed between the two N. ceranae populations in field conditions.

Dussaubat, Claudia Sagastume, Soledad Gomez-Moracho, Tamara Botías, Cristina García-Palencia, Pilar Martín-Hernández, Raquel Le Conte, Yves Higes, Mariano https://hdl.handle.net/10481/111449 2026-02-24T09:08:07Z

Comparative study of Nosema ceranae (Microsporidia) isolates from two different geographic origins Dussaubat, Claudia; Sagastume, Soledad; Gomez-Moracho, Tamara; Botías, Cristina; García-Palencia, Pilar; Martín-Hernández, Raquel; Le Conte, Yves; Higes, Mariano The intestinal honey bee parasite Nosema ceranae (Microsporidia) is at the root of colony losses in some regions while in others its presence causes no direct mortality. This is the case for Spain and France, respectively. It is hypothesized that differences in honey bee responses to N. ceranae infection could be due to the degree of virulence of N. ceranae strains from different geographic origins. To test this hypothesis, we first performed a study to compare the genetic variability of an rDNA fragment that could reveal differences between two N. ceranae isolates, one from Spain and one from France. Then we compared the infection capacity of both isolates in Apis mellifera iberiensis, based on the anatomopathological lesions due to N. ceranae development in the honey bee midgut, N. ceranae spore-load in the midgut and the honey bee survival rate. Our results suggest that there is no specific genetic background of the two N. ceranae isolates, from Spain or France, used in this study. These results agree with the infection development, honey bee survival and spore-loads that were similar between honey bees infected with both N. ceranae isolates. Probably, differences in honey bee response to infection are more related to the degree of tolerance of honey bee subspecies or local hybrids to N. ceranae, or experimental conditions in the case of laboratory trials, than to differences between N. ceranae isolates. Further studies should be done to estimate the contribution of each of these factors on the response of the honey bees to infection.

Higes, Mariano Gomez-Moracho, Tamara Rodriguez-García, Cristina Botías, Cristina Martín-Hernández, Raquel https://hdl.handle.net/10481/111424 2026-02-24T08:04:55Z

Preliminary effect of an experimental treatment with Nozevit®, (a phyto-pharmacological preparation) for Nosema ceranae control Higes, Mariano; Gomez-Moracho, Tamara; Rodriguez-García, Cristina; Botías, Cristina; Martín-Hernández, Raquel This study evaluates the efficacy of a natural product, Nozevit, for the treatment of nosemosis caused by Nosema ceranae, in the search for alternatives to fumagillin. To this end, a field study was conducted in two apiaries at the Marchamalo Agricultural Center. Colonies naturally infected with N. ceranae were treated with this product for several weeks in autumn, while control colonies received only sugar syrup.vThe presence of N. ceranae was assessed in both hive bees and forager bees before and after treatment. Each bee was individually analyzed by PCR to determine the progression of the parasitic infection. The results showed a non-significant trend toward a reduction in the percentage of infected forager bees. However, untreated colonies exhibited an increase in the proportion of infected hive bees, which could results in lower risk of collapse, making Nozevit an alternative to treat nosemosis type C. This is the authors accepted manuscript of an article published as the version of record in Journal of Apicultural Research © 2013 International Bee Research

Gomez-Moracho, Tamara Maside, Xulio Martín-Hernández, Raquel Higes, Mariano Bartolomé, Carolina https://hdl.handle.net/10481/111423 2026-02-24T08:03:02Z

High levels of genetic diversity in Nosema ceranae within Apis mellifera colonies Gomez-Moracho, Tamara; Maside, Xulio; Martín-Hernández, Raquel; Higes, Mariano; Bartolomé, Carolina Nosema ceranae is a widespread honeybee parasite, considered to be one of the pathogens involved in the colony losses phenomenon. To date, little is known about its intraspecific genetic variability. The few studies on N. ceranae variation have focused on the subunits of ribosomal DNA, which are not ideal for this purpose and have limited resolution. Here we characterized three single copy loci (Actin, Hsp70 and RPB1) in three N. ceranae isolates from Hungary and Hawaii. Our results provide evidence of unexpectedly high levels of intraspecific polymorphism, the coexistence of a wide variety of haplotypes within each bee colony, and the occurrence of genetic recombination in RPB1. Most haplotypes are not shared across isolates and derive from a few frequent haplotypes by a reduced number of singletons (mutations that appear usually just once in the sample), which suggest that they have a fairly recent origin. Overall, our data indicate that this pathogen has experienced a recent population expansion. The presence of multiple haplotypes within individual isolates could be explained by the existence of different strains of N. ceranae infecting honeybee colonies in the field which complicates, and must not be overlooked, further analysis of host–parasite interactions.

Gómez-Moracho, Tamara Heeb, Philip Lihoreau, Mathieu https://hdl.handle.net/10481/111042 2026-02-16T12:16:35Z

Effects of parasites and pathogens on bee cognition Gómez-Moracho, Tamara; Heeb, Philip; Lihoreau, Mathieu 1. Bees are key pollinators and their widespread decline has raised considerable concerns regarding the sustainability of ecosystems and food production. Many environmental stressors do not directly kill bees, but they alter their physiology and behaviour, ultimately impacting colonies and populations. 2. This review considers the impact of parasites and pathogens on bee cognition. 3. First the main parasites and pathogens of bees are described, as well as how they modify the foraging behaviour, learning and memory of their hosts. 4. Next, the various defence mechanisms developed by bees to mitigate these effects at both the individual and collective levels are examined. 5. Finally, there is a discussion on how integrating research on host parasites, animal behaviour and cognition will provide a more detailed assessment of the contribution of parasites and pathogens to declines in the bee population and help to inform constructive ecological interventions. We thank Darren Evans, James Gilbert and Gordon Port for inviting us to contribute to this special issue of Ecological Entomology. We also thank the editor and the two anonymous referees for their constructive comments on the manuscript. TGM is funded by a postdoctoral fellowship from the Fyssen Foundation. PH is funded by the ‘Laboratoire d’Excellence (LABEX)’ TULIP (ANR-10-LABX-41). ML is supported by the Centre National de la Recherche Scientifique (CNRS) and by grants from the IDEX of the University of Toulouse and the Agence Nationale de la Recherche (ANR-16-CE02-0002-01). The authors declare no conflict of interest.